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Modeling the Impact of Ex-Nido Transmitted Parasites on Ant Colony Dynamics

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Modeling the Impact of Ex-Nido Transmitted Parasites on Ant Colony Dynamics bioRxiv preprint doi: https://doi.org/10.1101/470575; this version posted November 14, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Modeling the impact of ex-nido transmitted parasites on ant colony dynamics Lauren E. Quevillon1,2, , David P. Hughes1,2,3∗, and Jessica M. Conway1,4∗ 1Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA, USA 2Department of Biology, Pennsylvania State University, University Park, PA, USA 3Department of Entomology, Pennsylvania State University, University Park, PA, USA 4Department of Mathematics, Pennsylvania State University, University Park, PA, USA ∗These authors contributed equally. Infectious disease outbreaks are a common constraint of group that these groups often live in extremely dense living con- living organisms. Ants (Hymenoptera: Formicidae) live in ditions with large colony sizes (up to millions of individu- large, dense colonies and are host to a diverse range of parasites als; (7), reviewed in (8)), and have an average higher genetic and pathogens, facilitating the possibility of epidemic-induced relatedness compared to other animal groups. This risk is collapse. However, the majority of parasites infecting ants re- further compounded by nesting habitats in soil and decaying quire a period of development outside of the nest before they wood that put colonies at increased risk of contact with mi- can transmit to their next ant host (‘ex-nido’ transmission) and crobial loads capable of causing disease (9). Additionally, the impact of these parasites on colony dynamics is unknown. Here we develop a mathematical model to assess ant colony dy- neighboring colonies overlap in their foraging ecology and namics in the presence of such parasites. We find that under compete for the same food resources, enhancing the potential field-realistic model conditions, such parasites are unlikely to for inter-colony transmission (10, 11). Indeed, social insects cause the epidemic collapse of mature ant colonies, unless colony are host to a diverse range of pathogens, parasites, and par- birth rate drops below 0.2328 ants/day. The preponderance of asitoids (hereafter ‘parasites’) (12, 13). However, ants and ex-nido transmitting parasites infecting ants and their limited other social insects have achieved incredible ecological suc- epidemiological impact on colony dynamics may partly explain cess (14, 15), and effectively managing their disease burden why collapsed ant colonies are rarely, if ever, observed in natu- could be one underlying reason for their continued success ral populations. over evolutionary time. social insects | ants | epidemiology | parasites Attempting to understand how social insects have contended Correspondence: [email protected] with considerable parasite pressure over their long evolution- ary history has driven empirical research during the past two Introduction decades. This work has uncovered many disease-fighting Infectious diseases capable of massive mortality events ap- mechanisms that social insects have in their arsenal, includ- pear to be an unavoidable consequence of living in large, ing physiological, behavioral, and organizational defenses at complex societies. As humans evolved from small groups of both the individual- and colony-levels (reviewed in (12, 16– hunter-gatherers into larger agrarian societies and then cities, 19)). Some mechanisms, such as allogrooming (the groom- we have seen an increase in the number of outbreaks that our ing of nest mates) (20, 21) and the transfer of immune mod- societies experience (1, 2). Some diseases (i.e. measles, sea- ulators or antibiotic secretions between nest mates (21, 22), sonal influenza) are ‘crowd diseases’ that can only be main- are evolutionary innovations following their transition to eu- tained because of large numbers of individuals living in close sociality, but it is likely that many of these immune mecha- proximity. Outbreaks readily occur in large natural and man- nisms were present prior to the transition to eusociality (23). aged animal populations as well. Boom-bust cycles in Gypsy Complementary theoretical studies have used a variety of moths driven by virus epidemics (3), Ebola and anthrax out- modeling frameworks to test the relative efficacies of these breaks amongst chimpanzees and gorillas (4, 5), and recur- mechanisms against parasites that are capable of direct trans- rent foot-and-mouth disease epizootics in commercial bovid mission from one infected nest mate to another. For example, all demonstrate that high density, group living organisms of- deterministic compartmental modeling has been used to as- ten contend with the steep costs of intense disease burden. sess differences in epidemiological outcomes when passive However, infectious disease outbreaks may not necessarily versus active immune modulators are passed between nest be an unavoidable consequence of evolving to live in dense mates (24), and how grooming, a behavioral defense used to groups. Social insects in the order Hymenoptera (ants, bees, remove infectious particles prior to infection, could impact and wasps), and the ants in particular, exemplify the liv- epidemic potential inside colonies (25). Others have used ing conditions that exaggerate the perceived risk of infec- individual-based modeling approaches to investigate how in- tious disease spread. These animal groups are defined by teraction heterogeneity (26), nest architecture (27), and im- eusociality, the highest form of social organization, in which munity and hygienic behavior (28) impact disease sever- there is a reproductive division of labor, overlapping gener- ity and colony survival. These modeling approaches have ations, and cooperative brood care (6). Eusociality means been very useful for comparing the relative efficacies of anti- Quevillon et al. | bioRχiv | November 14, 2018 | 1–25 bioRxiv preprint doi: https://doi.org/10.1101/470575; this version posted November 14, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. disease defenses against parasites that are capable of trans- colony dynamics and show that for a range of biological plau- mission inside the nest. sible parameter values, colony collapse is unlikely to occur. One key assumption underlying most of the above work is Finally we explore how other parameters (i.e. proportion of that parasites infecting ants are capable of direct, ant-to-ant the colony foraging, parasite developmental rate) impact the transmission inside the nest. However, the majority of para- potential impact of ex-nido parasitism on ant colony dynam- site species that infect ants have lifecycles that require a pe- ics. Our work suggests that disease dynamics in ant and other riod of development outside of the colony (‘ex-nido’), often social insect societies, in which ex-nido parasitism predomi- as free-living stages or in other host species, before they are nates rather than parasites directly transmitting between nest able to infect new hosts (Fig. 1) (12, 13). The amount of time mates, are fundamentally different from other social living such parasites need before they are capable of infecting a new organisms like mammals, which may partly explain the en- ant host varies considerably, from days to months or even during ecological success of the social insects. years. For example, following emergence from their ant host, phorid flies must mate and then find new hosts to oviposit Methods into within days (29). Trematodes infecting ants must com- plete development inside their vertebrate final host, mate and A. Model of ant colony dynamics in the presence and release eggs to be consumed by a snail before another ant can absence of ex-nido transmitting parasites. Our model be infected, a process which can take months (30). Finally, of mature ant colony dynamics in the presence and absence in temperate systems, the zombie-ant fungus Ophiocordyceps of ex-nido parasites is given by Eqs. (1-4) and summarized does not develop the sexual stages needed to release spores schematically in Fig. 2. In the absence of parasitism, we and infect new ants until many months following the death of make the simplifying assumption that there are three devel- its original ant host (31). Thus, with these ‘ex-nido’ parasites, opmental and sociological castes (compartments) that indi- direct transmission between nest mates inside colonies is not viduals transition through in ant colonies, listed below: possible, potentially precluding the threat of major disease outbreaks inside colonies. • Brood (B): a period of biological development during Fig. 1. Transmission strategies used by parasites infecting ants. which individuals transition from egg through several larval stages. Direct transmission Indirect transmission • Nest workers (N): a variable period of time during (One host) (Two or more hosts) which individuals participate in intranidal tasks such as brood care and nest maintenance. ex-nido • Foragers (Fs): a variable period of time that older ants in-nido transition into according to colony need; foraging ants gather food and participate in extranidal territory de- ex-nido fense and maintenance, which puts them
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